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Oxidative Medicine and Cellular Longevity
Volume 2017, Article ID 3724545, 13 pages
https://doi.org/10.1155/2017/3724545
Research Article

Glycosides from Stevia rebaudiana Bertoni Possess Insulin-Mimetic and Antioxidant Activities in Rat Cardiac Fibroblasts

1Department of Pharmacy and Biotechnology, Alma Mater Studiorum, University of Bologna, Via Irnerio, No. 48, 40126 Bologna, Italy
2Department for Life Quality Studies, Alma Mater Studiorum, University of Bologna, Corso d’Augusto, No. 237, 47921 Rimini, Italy
3Department of Surgery, Medicine, Dentistry and Morphological Sciences, University of Modena and Reggio Emilia, Policlinico, Via del Pozzo, No. 71, 41124 Modena, Italy
4School of Pharmacy, University of Camerino, Via Gentile III da Varano, 62032 Camerino, Italy
5Department of Medical Sciences, University of Ferrara, Via Luigi Borsari, No. 46, 44121 Ferrara, Italy

Correspondence should be addressed to Diana Fiorentini; ti.obinu@initneroif.anaid

Received 31 May 2017; Accepted 11 July 2017; Published 30 August 2017

Academic Editor: Angela Marino

Copyright © 2017 Cecilia Prata et al. This is an open access article distributed under the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.

Linked References

  1. R. Lemus-Mondaca, A. Vega-Galvez, L. Zura-Bravo, and K. Ah-Hen, “Stevia rebaudiana Bertoni, source of a high potency natural sweetener: a comprehensive review on the biochemical, nutritional and functional aspects,” Food Chemistry, vol. 132, no. 3, pp. 1121–1132, 2012. View at Publisher · View at Google Scholar · View at Scopus
  2. S. Purkayastha, A. Markosyan, I. Prakash et al., “Steviol glycosides in purified stevia leaf extract sharing the same metabolic fate,” Regulatory Toxicology and Pharmacology, vol. 77, pp. 125–133, 2016. View at Publisher · View at Google Scholar · View at Scopus
  3. U. Wolwer-Rieck, “The leaves of Stevia rebaudiana (Bertoni), their constituents and the analyses thereof: a review,” Journal of Agricultural and Food Chemistry, vol. 60, no. 4, pp. 886–895, 2012. View at Publisher · View at Google Scholar · View at Scopus
  4. D. D. Soejarto, A. D. Kinghorn, and N. R. Farnsworth, “Potential sweetening agents of plant origin. III. Organoleptic evaluation of Stevia leaf herbarium samples for sweetness,” Journal of Natural Products, vol. 45, no. 5, pp. 590–599, 1982. View at Publisher · View at Google Scholar
  5. G. Brahmachari, L. C. Mandal, R. Roy, S. Mondal, and A. K. Brahmachari, “Stevioside and related compounds - molecules of pharmaceutical promise: a critical overview,” Archiv der Pharmazie (Weinheim, Germany), vol. 344, no. 1, pp. 5–19, 2011. View at Publisher · View at Google Scholar · View at Scopus
  6. J. M. Geuns, “Stevioside,” Phytochemistry, vol. 64, no. 5, pp. 913–921, 2003. View at Publisher · View at Google Scholar · View at Scopus
  7. G. F. Ferrazzano, T. Cantile, B. Alcidi et al., “Is Stevia rebaudiana Bertoni a non cariogenic sweetener? A review,” Molecules, vol. 21, no. 1, article E38, 2015. View at Publisher · View at Google Scholar · View at Scopus
  8. A. D. Kinghorn, N. Kaneda, N. I. Baek, E. J. Kennelly, and D. D. Soejarto, “Noncariogenic intense natural sweeteners,” Medicinal Research Reviews, vol. 18, no. 5, pp. 347–360, 1998. View at Publisher · View at Google Scholar
  9. J. C. Ruiz-Ruiz, Y. B. Moguel-Ordonez, and M. R. Segura-Campos, “Biological activity of Stevia rebaudiana Bertoni and their relationship to health,” Critical Reviews in Food Science and Nutrition, vol. 57, 2015. View at Publisher · View at Google Scholar
  10. V. Chatsudthipong and C. Muanprasat, “Stevioside and related compounds: therapeutic benefits beyond sweetness,” Pharmacology & Therapeutics, vol. 121, no. 1, pp. 41–54, 2009. View at Publisher · View at Google Scholar · View at Scopus
  11. S. K. Goyal, R. Samsher, and K. Goyal, “Stevia (Stevia rebaudiana) a bio-sweetener: a review,” International Journal of Food Sciences and Nutrition, vol. 61, no. 1, pp. 1–10, 2010. View at Publisher · View at Google Scholar · View at Scopus
  12. C. Boonkaewwan, C. Toskulkao, and M. Vongsakul, “Anti-inflammatory and immunomodulatory activities of stevioside and its metabolite steviol on THP-1 cells,” Journal of Agricultural and Food Chemistry, vol. 54, no. 3, pp. 785–789, 2006. View at Publisher · View at Google Scholar · View at Scopus
  13. C. European Food Safety Authority, “Revised exposure assessment for steviol glycosides for the proposed uses as a food additive,” EFSA Journal, vol. 9, no. 1, p. 1972, 2011. View at Publisher · View at Google Scholar
  14. J. D. Urban, M. C. Carakostas, and S. L. Taylor, “Steviol glycoside safety: are highly purified steviol glycoside sweeteners food allergens?” Food and Chemical Toxicology, vol. 75, pp. 71–78, 2015. View at Publisher · View at Google Scholar · View at Scopus
  15. WHO, “WHO expert committee on diabetes mellitus,” World Health Organization Technical Report Series, vol. 916, p. 160, 2003. View at Google Scholar
  16. N. H. Mohd-Radzman, W. I. W. Ismail, Z. Adam, S. S. Jaapar, and A. Adam, “Potential roles of Stevia rebaudiana Bertoni in abrogating insulin resistance and diabetes: a review,” Evidence-based Complementary and Alternative Medicine, vol. 2013, Article ID 718049, 10 pages, 2013. View at Publisher · View at Google Scholar · View at Scopus
  17. P. B. Jeppesen, S. Gregersen, C. R. Poulsen, and K. Hermansen, “Stevioside acts directly on pancreatic beta cells to secrete insulin: actions independent of cyclic adenosine monophosphate and adenosine triphosphate-sensitive K+-channel activity,” Metabolism, vol. 49, no. 2, pp. 208–214, 2000. View at Publisher · View at Google Scholar
  18. R. Abudula, V. V. Matchkov, P. B. Jeppesen, H. Nilsson, C. Aalkjaer, and K. Hermansen, “Rebaudioside A directly stimulates insulin secretion from pancreatic beta cells: a glucose-dependent action via inhibition of ATP-sensitive K-channels,” Diabetes, Obesity & Metabolism, vol. 10, no. 11, pp. 1074–1085, 2008. View at Publisher · View at Google Scholar · View at Scopus
  19. J. C. Chang, M. C. Wu, I. M. Liu, and J. T. Cheng, “Increase of insulin sensitivity by stevioside in fructose-rich chow-fed rats,” Hormone and Metabolic Research, vol. 37, no. 10, pp. 610–616, 2005. View at Publisher · View at Google Scholar · View at Scopus
  20. P. B. Jeppesen, S. Gregersen, K. K. Alstrup, and K. Hermansen, “Stevioside induces antihyperglycaemic, insulinotropic and glucagonostatic effects in vivo: studies in the diabetic Goto-Kakizaki (GK) rats,” Phytomedicine, vol. 9, no. 1, pp. 9–14, 2002. View at Publisher · View at Google Scholar
  21. S. Gregersen, P. B. Jeppesen, J. J. Holst, and K. Hermansen, “Antihyperglycemic effects of stevioside in type 2 diabetic subjects,” Metabolism, vol. 53, no. 1, pp. 73–76, 2004. View at Publisher · View at Google Scholar · View at Scopus
  22. M. Ritu and J. Nandini, “Nutritional composition of Stevia rebaudiana- a sweet herb and its hypoglycaemic and hypolipidaemic effect on patients with non insulin dependent diabetes mellitus,” Journal of the Science of Food and Agriculture, vol. 96, 2016. View at Publisher · View at Google Scholar · View at Scopus
  23. S. Bhasker, H. Madhav, and M. Chinnamma, “Molecular evidence of insulinomimetic property exhibited by steviol and stevioside in diabetes induced L6 and 3T3L1 cells,” Phytomedicine, vol. 22, no. 11, pp. 1037–1044, 2015. View at Publisher · View at Google Scholar · View at Scopus
  24. C. Bender, S. Graziano, and B. F. Zimmermann, “Study of Stevia rebaudiana Bertoni antioxidant activities and cellular properties,” International Journal of Food Sciences and Nutrition, vol. 66, no. 5, pp. 553–558, 2015. View at Publisher · View at Google Scholar · View at Scopus
  25. S. Ghanta, A. Banerjee, A. Poddar, and S. Chattopadhyay, “Oxidative DNA damage preventive activity and antioxidant potential of Stevia rebaudiana (Bertoni) Bertoni, a natural sweetener,” Journal of Agricultural and Food Chemistry, vol. 55, no. 26, pp. 10962–10967, 2007. View at Publisher · View at Google Scholar · View at Scopus
  26. N. Shivanna, M. Naika, F. Khanum, and V. K. Kaul, “Antioxidant, anti-diabetic and renal protective properties of Stevia rebaudiana,” Journal of Diabetes and its Complications, vol. 27, no. 2, pp. 103–113, 2013. View at Publisher · View at Google Scholar · View at Scopus
  27. S. Singh, V. Garg, and D. Yadav, “Antihyperglycemic and antioxidative ability of Stevia rebaudiana (Bertoni) leaves in diabetes induced mice,” International Journal of Pharmacy and Pharmaceutical Sciences, vol. 5, no. 2, pp. 297–302, 2013. View at Google Scholar
  28. B. Rizzo, L. Zambonin, C. Angeloni et al., “Steviol glycosides modulate glucose transport in different cell types,” Oxidative Medicine and Cellular Longevity, vol. 2013, Article ID 348169, 11 pages, 2013. View at Publisher · View at Google Scholar · View at Scopus
  29. D. Zhang, Y. Cui, B. Li, X. Luo, B. Li, and Y. Tang, “miR-155 regulates high glucose-induced cardiac fibrosis via the TGF-beta signaling pathway,” Molecular BioSystems, vol. 13, no. 1, pp. 215–224, 2016. View at Publisher · View at Google Scholar
  30. G. Pandini, F. Frasca, R. Mineo, L. Sciacca, R. Vigneri, and A. Belfiore, “Insulin/insulin-like growth factor I hybrid receptors have different biological characteristics depending on the insulin receptor isoform involved,” The Journal of Biological Chemistry, vol. 277, no. 42, pp. 39684–39695, 2002. View at Publisher · View at Google Scholar · View at Scopus
  31. K. Reiss, W. Cheng, J. Kajstura, E. H. Sonnenblick, L. G. Meggs, and P. Anversa, “Fibroblast proliferation during myocardial development in rats is regulated by IGF-1 receptors,” The American Journal of Physiology, vol. 269, 3, Part 2, pp. H943–H951, 1995. View at Google Scholar
  32. N. Longo, G. I. Bell, R. C. Shuster, L. D. Griffin, S. D. Langley, and L. J. Elsas, “Human fibroblasts express the insulin-responsive glucose transporter (GLUT4),” Transactions of the Association of American Physicians, vol. 103, pp. 202–213, 1990. View at Google Scholar
  33. S. Hrelia, D. Fiorentini, T. Maraldi et al., “Doxorubicin induces early lipid peroxidation associated with changes in glucose transport in cultured cardiomyocytes,” Biochimica et Biophysica Acta, vol. 1567, no. 1-2, pp. 150–156, 2002. View at Google Scholar
  34. L. H. Johansson and L. A. Borg, “A spectrophotometric method for determination of catalase activity in small tissue samples,” Analytical Biochemistry, vol. 174, no. 1, pp. 331–336, 1988. View at Publisher · View at Google Scholar · View at Scopus
  35. T. Maraldi, C. Prata, D. Fiorentini, L. Zambonin, L. Landi, and G. Hakim, “Induction of apoptosis in a human leukemic cell line via reactive oxygen species modulation by antioxidants,” Free Radical Biology & Medicine, vol. 46, no. 2, pp. 244–252, 2009. View at Publisher · View at Google Scholar · View at Scopus
  36. L. Schaffer, C. L. Brand, B. F. Hansen et al., “A novel high-affinity peptide antagonist to the insulin receptor,” Biochemical and Biophysical Research Communications, vol. 376, no. 2, pp. 380–383, 2008. View at Publisher · View at Google Scholar · View at Scopus
  37. Y. Benomar, N. Naour, A. Aubourg et al., “Insulin and leptin induce Glut4 plasma membrane translocation and glucose uptake in a human neuronal cell line by a phosphatidylinositol 3-kinase- dependent mechanism,” Endocrinology, vol. 147, no. 5, pp. 2550–2556, 2006. View at Publisher · View at Google Scholar · View at Scopus
  38. H. X. Chen and E. Sharon, “IGF-1R as an anti-cancer target—trials and tribulations,” Chinese Journal of Cancer, vol. 32, no. 5, pp. 242–252, 2013. View at Publisher · View at Google Scholar · View at Scopus
  39. D. Chanda, J. J. Luiken, and J. F. Glatz, “Signaling pathways involved in cardiac energy metabolism,” FEBS Letters, vol. 590, no. 15, pp. 2364–2374, 2016. View at Publisher · View at Google Scholar · View at Scopus
  40. N. H. Mohd-Radzman, W. I. W. Ismail, S. S. Jaapar, Z. Adam, and A. Adam, “Stevioside from Stevia rebaudiana Bertoni increases insulin sensitivity in 3T3-L1 adipocytes,” Evidence-based Complementary and Alternative Medicine, vol. 2013, Article ID 938081, 8 pages, 2013. View at Publisher · View at Google Scholar · View at Scopus
  41. P. Singh, J. M. Alex, and F. Bast, “Insulin receptor (IR) and insulin-like growth factor receptor 1 (IGF-1R) signaling systems: novel treatment strategies for cancer,” Medical Oncology, vol. 31, no. 1, p. 805, 2014. View at Publisher · View at Google Scholar · View at Scopus
  42. A. Belfiore, F. Frasca, G. Pandini, L. Sciacca, and R. Vigneri, “Insulin receptor isoforms and insulin receptor/insulin-like growth factor receptor hybrids in physiology and disease,” Endocrine Reviews, vol. 30, no. 6, pp. 586–623, 2009. View at Publisher · View at Google Scholar · View at Scopus
  43. L. Knudsen, B. F. Hansen, P. Jensen et al., “Agonism and antagonism at the insulin receptor,” PLoS One, vol. 7, no. 12, article e51972, 2013. View at Publisher · View at Google Scholar · View at Scopus
  44. A. Chowdhury, L. Hasselbach, F. Echtermeyer, N. Jyotsana, G. Theilmeier, and C. Herzog, “Fibulin-6 regulates pro-fibrotic TGF-beta responses in neonatal mouse ventricular cardiac fibroblasts,” Scientific Reports, vol. 7, article 42725, 2017. View at Publisher · View at Google Scholar
  45. D. L. Coven, X. Hu, L. Cong et al., “Physiological role of AMP-activated protein kinase in the heart: graded activation during exercise,” American Journal of Physiology Endocrinology and Metabolism, vol. 285, no. 3, pp. E629–E636, 2003. View at Publisher · View at Google Scholar
  46. J. S. Fisher, “Potential role of the AMP-activated protein kinase in regulation of insulin action,” Cell, vol. 2, no. 3, pp. 68–81, 2006. View at Google Scholar
  47. J. W. Baynes and S. R. Thorpe, “Role of oxidative stress in diabetic complications: a new perspective on an old paradigm,” Diabetes, vol. 48, no. 1, pp. 1–9, 1999. View at Publisher · View at Google Scholar · View at Scopus
  48. S. P. Wolff and R. T. Dean, “Glucose autoxidation and protein modification. The potential role of ‘autoxidative glycosylation’ in diabetes,” The Biochemical Journal, vol. 245, no. 1, pp. 243–250, 1987. View at Publisher · View at Google Scholar
  49. J. L. Rains and S. K. Jain, “Oxidative stress, insulin signaling, and diabetes,” Free Radical Biology & Medicine, vol. 50, no. 5, pp. 567–575, 2011. View at Publisher · View at Google Scholar · View at Scopus
  50. K. L. Wolfe and R. H. Liu, “Cellular antioxidant activity (CAA) assay for assessing antioxidants, foods, and dietary supplements,” Journal of Agricultural and Food Chemistry, vol. 55, no. 22, pp. 8896–8907, 2007. View at Publisher · View at Google Scholar · View at Scopus
  51. C. Angeloni, M. Malaguti, and S. Hrelia, “Antiglycative activity of sulforaphane: a new avenue to counteract neurodegeneration?” Neural Regeneration Research, vol. 10, no. 11, pp. 1750-1751, 2015. View at Publisher · View at Google Scholar · View at Scopus
  52. L. Vasko, J. Vaskova, A. Fejercakova, G. Mojžišová, and J. Poráčová, “Comparison of some antioxidant properties of plant extracts from Origanum vulgare, Salvia officinalis, Eleutherococcus senticosus and Stevia rebaudiana,” In Vitro Cellular & Developmental Biology - Animal, vol. 50, no. 7, pp. 614–622, 2014. View at Publisher · View at Google Scholar · View at Scopus
  53. C. N. Hao, Y. J. Geng, F. Li et al., “Insulin-like growth factor-1 receptor activation prevents hydrogen peroxide-induced oxidative stress, mitochondrial dysfunction and apoptosis,” Apoptosis, vol. 16, no. 11, pp. 1118–1127, 2011. View at Publisher · View at Google Scholar · View at Scopus
  54. C. A. Souders, S. L. Bowers, and T. A. Baudino, “Cardiac fibroblast: the renaissance cell,” Circulation Research, vol. 105, no. 12, pp. 1164–1176, 2009. View at Publisher · View at Google Scholar · View at Scopus